Function or Drive – Why are the Accessory Chromosomes of Zymoseptoria tritici maintained?

The genome of the fungal wheat pathogen Zymoseptoria tritici comprises a set of accessory chromosomes that has persisted at least since the speciation of Z. tritici approx. 11,000 years ago. The long-term maintenance of these chromosomes is at odds with the frequently observed loss of one or more of these chromosomes in isolates collected in a wide variety of environments. Here we performed two types of experiments to address the functional role and the underlying mechanisms of the maintenance of accessory chromosomes in Z. tritici. We tested the functional relevance of these chromosomes using a forward genetics approach based on isogenic whole chromosome deletion strains in the reference isolate IPO323. Surprisingly, the presence of accessory chromosomes is associated with a fitness cost in planta, but dependent on the host genotype. An associated fitness cost should favor complete loss, not maintenance, of the chromosomes in the fungal population. However, additional mating experiments in planta between isolates differing in their set of accessory chromosomes subsequently revealed a possible explanation for the chromosomes’ persistence. Unpaired accessory chromosomes, i.e. present only in one parental strain, are found to segregate in a non-mendelian manner during meiosis, leading to an overrepresentation of these unpaired accessory chromosomes in the resulting ascospores. Moreover, this segregation distortion was shown to be the result of a female meiotic drive, which was in turn influenced by environmental factors. We conclude that the maintenance of the accessory chromosomes in the fungal population is caused by meiotic drive and suggest that these chromosomes represent a novel group of selfish genetic elements.